The sense of smell, its signalling pathways, and the dichotomy of cilia and microvilli in olfactory sensory cells

BMC Neuroscience

Volumn 8, Issue SUPPL. 3, 2007, Pages

  Elsaesser, Rebecca ^a   Paysan, Jacques ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; NEUROPEPTIDE Y;

FOOD PREFERENCE; HUMAN; MICROVILLUS; NEURAL STEM CELL; NONHUMAN; ODOR; OLFACTORY DISCRIMINATION; OLFACTORY EPITHELIUM; OLFACTORY NERVOUS SYSTEM; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PHOTORECEPTOR CELL; PHYLOGENETIC TREE; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SMELLING; SOCIAL LEARNING; ANIMAL; EUKARYOTIC FLAGELLUM; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; CILIA; HUMANS; MICROVILLI; OLFACTORY MUCOSA; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; SIGNAL TRANSDUCTION; SMELL;

EID: 38449108407     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-8-S3-S1     Document Type: Review

References (157)

1. McCoy E The emperor of wine: The rise of Robert M. Parker, Jr. and the reign of American taste New York: ECCO 1 2005.
2. Morrot G Brochet F Dubourdieu D The color of odors Brain Lang 2001, 79(2):309-320. 10.1006/brln.2001.2493 11712849
3. Cain WS Know with the Nose - Keys to Odor Identification Science 1979, 203(4379):467-470. 10.1126/science.760202 760202
4. Dravnieks A Masurat T Lamm RA Hedonics of Odors and Odor Descriptors Journal of the Air Pollution Control Association 1984, 34(7):752-755.
5. Zald DH Pardo JV Emotion, olfaction, and the human amygdala: Amygdala activation during aversive olfactory stimulation Proceedings of the National Academy of Sciences of the United States of America 1997, 94(8):4119-4124. 20578 9108115 10.1073/pnas.94.8.4119
6. AlaouiIsmaili O VernetMaury E Dittmar A Delhomme G Chanel J Odor hedonics: Connection with emotional response estimated by autonomic parameters Chemical Senses 1997, 22(3):237-248. 10.1093/chemse/22.3.237 9218136
7. Vernet-Maury E Alaoui-Ismaili O Dittmar A Delhomme G Chanel J Basic emotions induced by odorants: A new approach based on autonomic pattern results Journal of the Autonomic Nervous System 1999, 75(2-3):176-183. 10.1016/S0165-1838(98)00168-4 10189120
8. García Márquez G The story of a shipwrecked sailor: Who drifted on a life raft for ten days without food or water, was proclaimed a national hero, kissed by beauty queens, made rich through publicity, and then spurned by the government and forgotten for all time. 1st Vintage Books edition New York: Vintage Books 1987.
9. Maletzky BM Steinhauser C Olfactory aversion and its mechanism of action represents an excellent summary of this useful technique Sex Abuse 2003, 15(3):215-217. 10.1023/A:1023503501408 12889325
10. Laws DR Olfactory aversion: Notes on procedure, with speculations on its mechanism of effect Sex Abuse 2001, 13(4):275-287. 10.1023/ A:1017522515854 11677928
11. Robinson J Robinson J How to taste: A guide to enjoying wine New York: Simon & Schuster 2000.
12. Zhu M Ahlberg PE The origin of the internal nostril of tetrapods Nature 2004, 432(7013):94-97. 10.1038/nature02843 15525987
13. Zuker CS Neuron Satellite Meeting. Washington DC 2005.
14. Drewnowski A The science and complexity of bitter taste Nutrition Reviews 2001, 59(6):163-169. 11444592
15. Octopus Publishing Group Limited Complete Indian Cooking. U.S. edition London New York, NY: Hamlyn 1999.
16. Galef BG Lee WY Whiskin EE Lack of interference in long-term memory for socially learned food preferences in rats (Rattus norvegicus) Journal of Comparative Psychology 2005, 119(2):131-135. 10.1037/0735-7036.119.2.131 15982156
17. Baker BJ Booth DA Genuinely Olfactory Preferences Conditioned by Protein Repletion Appetite 1989, 13(3):223-227. 10.1016/0195-6663(89)90015-9 2596844
18. Mueller KL Hoon MA Erlenbach I Chandrashekar J Zuker CS Ryba NJP The receptors and coding logic for bitter taste Nature 2005, 434(7030):225-229. 10.1038/nature03352 15759003
19. Elsaesser R Paysan A Morituri te salutant? Olfactory signal transduction and the role of phosphoinositides Journal of Neurocytology 2005, 34(1-2):97-116. 10.1007/s11068-005-5050-z 16374712
20. Hrazdina G Aroma production by tissue cultures J Agric Food Chem 2006, 54(4):1116-1123. 10.1021/jf053146w 16478225
21. Lin DY Zhang SZ Block E Katz LC Encoding social signals in the mouse main olfactory bulb Nature 2005, 434(7032):470-477. 10.1038/nature03414 15724148
22. Brun JP The production of perfumes in antiquity: The cases of Delos and Paestum American Journal of Archaeology 2000, 104(2):277-308. 10.2307/ 507452
23. Debonoayrout J Perfume-Making in Ancient Egypt Historia 1995, 588:48-53.
24. Mitchell MA Edman WW Konigsbacher KS Importance of Odor as Nonfunctional Component or Odor-Tool of Marketing Annals of the New York Academy of Sciences 1964, 116(A2):685. 10.1111/j.1749-6632.1964.tb45103.x 14220566
25. Zou ZH Buck LB Combinatorial effects of odorant mixes in olfactory cortex Science 2006, 311(5766):1477-1481. 10.1126/science.1124755 16527983
26. Zou ZH Li FS Buck LB Odor maps in the olfactory cortex Proceedings of the National Academy of Sciences of the United States of America 2005, 102(21):7724-7729. 1138263 15911779 10.1073/pnas.0503027102
27. Laurent G A systems perspective on early olfactory coding Science 1999, 286(5440):723-728. 10.1126/science.286.5440.723 10531051
28. Laurent G Olfactory network dynamics and the coding of multidimensional signals Nature Reviews Neuroscience 2002, 3(11):884-895. 10.1038/nrn964 12415296
29. Horowitz LF Montmayeur JP Echelard Y Buck LB A genetic approach to trace neural circuits Proceedings of the National Academy of Sciences of the United States of America 1999, 96(6):3194-3199. 15918 10077660 10.1073/ pnas.96.6.3194
30. Zou ZH Horowitz LF Montmayeur JP Snapper S Buck LB Genetic tracing reveals a stereotyped sensory map in the olfactory cortex Nature 2001, 414(6860):173-179. 10.1038/35102506 11700549
31. Boehm U Zou ZH Buck LB Feedback loops link odor and pheromone signaling with reproduction Cell 2005, 123(4):683-695. 10.1016/j.cell.2005.09.027 16290036
32. Gottfried JA Dolan RJ The nose smells what the eye sees: Crossmodal visual facilitation of human olfactory perception Neuron 2003, 39(2):375-386. 10.1016/S0896-6273(03)00392-1 12873392
33. Gottfried JA Smith APR Rugg MD Dolan RJ Remembrance of odors past: Human olfactory cortex in cross-modal recognition memory Neuron 2004, 42(4):687-695. 10.1016/S0896-6273(04)00270-3 15157428
34. Gottfried JA Winston JS Dolan RJ Dissociable codes of odor quality and odorant structure in human piriform cortex Neuron 2006, 49(3):467-479. 10.1016/j.neuron.2006.01.007 16446149
35. Osterbauer RA Matthews PM Jenkinson M Beckmann CF Hansen PC Calvert GA Color of scents: Chromatic stimuli modulate odor responses in the human brain Journal of Neurophysiology 2005, 93(6):3434-3441. 10.1152/ jn.00555.2004 15689393
36. Castriota-Scanderbeg A Hagberg GE Cerasa A Committeri G Galati G Patria F Pitzalis S Caltagirone C Frackowlak R The appreciation of wine by sommeliers: A functional magnetic resonance study of sensory integration Neuroimage 2005, 25(2):570-578. 10.1016/j.neuroimage.2004.11.045 15784436
37. Laurent G Olfactory processing: Maps, time and codes Current Opinion in Neurobiology 1997, 7(4):547-553. 10.1016/S0959-4388(97)80035-9 9287196
38. Laurent G Wehr M Davidowitz H Temporal representations of odors in an olfactory network Journal of Neuroscience 1996, 16(12):3837-3847. 8656278
39. Stopfer M Jayaraman V Laurent G Intensity versus identity coding in an olfactory system Neuron 2003, 39(6):991-1004. 10.1016/ j.neuron.2003.08.011 12971898
40. Amoore JE Odor theory and odor classification Fragrance chemistry: The science of the sense of smell New York: Academic Press Theimer ET 1982:27-76.
41. Buck L Axel R A novel multigene family may encode odorant receptors: A molecular basis for odor recognition Cell 1991, 65(1):175-187. 10.1016/ 0092-8674(91)90418-X 1840504
42. Chess A Buck L Dowling MM Axel R Ngai J Molecular biology of smell: expression of the multigene family encoding putative odorant receptors Cold Spring Harb Symp Quant Biol 1992, 57:505-516. 1339687
43. Touhara K Odor discrimination by G protein-coupled olfactory receptors Microsc Res Tech 2002, 58(3):135-141. 10.1002/jemt.10131 12203691
44. Serizawa S Miyamichi K Sakano H One neuron-one receptor rule in the mouse olfactory system Trends Genet 2004, 20(12):648-653. 10.1016/ j.tig.2004.09.006 15522461
45. Reed RR After the holy grail: Establishing a molecular basis for Mammalian olfaction Cell 2004, 116(2):329-336. 10.1016/ S0092-8674(04)00047-9 14744441
46. Matthews HR Reisert J Calcium, the two-faced messenger of olfactory transduction and adaptation Curr Opin Neurobiol 2003, 13(4):469-475. 10.1016/S0959-4388(03)00097-7 12965295
47. Ronnett GV Moon C G proteins and olfactory signal transduction Annu Rev Physiol 2002, 64:189-222. 10.1146/annurev.physiol.64.082701.102219 11826268
48. Frings S Chemoelectrical signal transduction in olfactory sensory neurons of air-breathing vertebrates Cell Mol Life Sci 2001, 58(4):510-519. 10.1007/PL00000876 11361086
49. Gold GH Controversial issues in vertebrate olfactory transduction Annu Rev Physiol 1999, 61:857-871. 10.1146/annurev.physiol.61.1.857 10099713
50. Schild D Restrepo D Transduction mechanisms in vertebrate olfactory receptor cells Physiol Rev 1998, 78(2):429-466. 9562035
51. Ebrahimi FA Chess A Olfactory G proteins: Simple and complex signal transduction Curr Biol 1998, 8(12):R431-433. 10.1016/ S0960-9822(98)70271-4 9637917
52. Firestein S How the olfactory system makes sense of scents Nature 2001, 413(6852):211-218. 10.1038/35093026 11557990
53. Menini A Lagostena L Boccaccio A Olfaction: From odorant molecules to the olfactory cortex News Physiol Sci 2004, 19:101-104. 15143202
54. Paysan J Breer H Molecular physiology of odor detection: Current views Pflugers Archiv-European Journal of Physiology 2001, 441(5):579-586. 10.1007/s004240000492 11294238
55. Buck LB Olfactory receptors and odor coding in mammals Nutr Rev 2004, 62(11 Pt 2):S184-188. discussion S224-141 10.1301/nr.2004.nov.S184-S188 15630933
56. Mombaerts P Wang F Dulac C Vassar R Chao SK Nemes A Mendelsohn M Edmondson J Axel R The molecular biology of olfactory perception Cold Spring Harb Symp Quant Biol 1996, 61:135-145. 9246442
57. Menco BPM Ciliated and Microvillous Structures of Rat Olfactory and Nasal Respiratory Epithelia - a Study Using Ultra-Rapid Cryo-Fixation Followed by Freeze-Substitution or Freeze-Etching Cell and Tissue Research 1984, 235(2):225-241. 10.1007/BF00217846
58. Reuter D Zierold K Schroder W Frings S Contribution of chloride to receptor current in olfactory neurons: Cl-equilibrium potential and ionic composition of olfactory mucus European Journal of Neuroscience 1998, 10:360-360.
59. Reuter D Zierold K Schroder WH Frings S A depolarizing chloride current contributes to chemoelectrical transduction in olfactory sensory neurons in situ Journal of Neuroscience 1998, 18(17):6623-6630. 9712634
60. Smith JJ Travis SM Greenberg EP Welsh MJ Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid Cell 1996, 85(2):229-236. 10.1016/S0092-8674(00)81099-5 8612275
61. Tarran R Trout L Donaldson SH Boucher RC Soluble mediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia Journal of General Physiology 2006, 127(5):591-604. 10.1085/jgp.200509468 16636206
62. Duchamp-Viret P Chaput MA Duchamp A Odor response properties of rat olfactory receptor neurons Science 1999, 284(5423):2171-2174. 10.1126/ science.284.5423.2171 10381881
63. Duchamp-Viret P Duchamp A Chaput MA Peripheral odor coding in the rat and frog: Quality and intensity specification Journal of Neuroscience 2000, 20(6):2383-2390. 10704512
64. Duchamp-Viret P Duchamp A Chaput MA Single olfactory sensory neurons simultaneously integrate the components of an odour mixture European Journal of Neuroscience 2003, 18(10):2690-2696. 10.1111/ j.1460-9568.2003.03001.x 14656317
65. Mombaerts P Molecular biology of odorant receptors in vertebrates Annu Rev Neurosci 1999, 22:487-509. 10.1146/annurev.neuro.22.1.487 10202546
66. Pace U Hanski E Salomon Y Lancet D Odorant-sensitive adenylate cyclase may mediate olfactory reception Nature 1985, 316(6025):255-258. 10.1038/ 316255a0 3927168
67. Kaupp UB Seifert R Cyclic nucleotide-gated ion channels Physiol Rev 2002, 82(3):769-824. 12087135
68. Restrepo D The ins and outs of intracellular chloride in olfactory receptor neurons Neuron 2005, 45(4):481-482. 10.1016/ j.neuron.2005.02.002 15721233
69. Reisert J Lai J Yau KW Bradley J Mechanism of the excitatory Cl-response in mouse olfactory receptor neurons Neuron 2005, 45(4):553-561. 10.1016/ j.neuron.2005.01.012 15721241
70. Zufall F Leinders-Zufall T The cellular and molecular basis of odor adaptation Chem Senses 2000, 25(4):473-481. 10.1093/chemse/25.4.473 10944513
71. Bhandawat V Reisert J Yau KW Elementary response of olfactory receptor neurons to odorants Science 2005, 308(5730):1931-1934. 10.1126/ science.1109886 15976304
72. Ache BW Zhainazarov A Dual 2Nd-Messenger Pathways in Olfactory Transduction Current Opinion in Neurobiology 1995, 5(4):461-466. 10.1016/ 0959-4388(95)80006-9 7488847
73. Breer H 2Nd Messenger Signaling in Olfaction Ciba Foundation Symposia 1993, 179:97-114. 8168385
74. Sklar PB Anholt RR Snyder SH The odorant-sensitive adenylate cyclase of olfactory receptor cells. Differential stimulation by distinct classes of odorants J Biol Chem 1986, 261(33):15538-15543. 3536906
75. Boekhoff I Tareilus E Strotmann J Breer H Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants Embo J 1990, 9(8):2453-2458. 552272 2164471
76. Breer H Boekhoff I Tareilus E Rapid kinetics of second messenger formation in olfactory transduction Nature 1990, 345(6270):65-68. 10.1038/345065a0 2158631
77. Raming K Krieger J Strotmann J Boekhoff I Kubick S Baumstark C Breer H Cloning and expression of odorant receptors Nature 1993, 361(6410):353-356. 10.1038/361353a0 7678922
78. Barinaga M Mutant mice and worms help solve mysteries of olfaction Science 1996, 274(5287):500-501. 10.1126/science.274.5287.500 8928002
79. Belluscio L Gold GH Nemes A Axel R Mice deficient in G(olf) are anosmic Neuron 1998, 20(1):69-81. 10.1016/S0896-6273(00)80435-3 9459443
80. Wong ST Trinh K Hacker B Chan GC Lowe G Gaggar A Xia Z Gold GH Storm DR Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice Neuron 2000, 27(3):487-497. 10.1016/S0896-6273(00)00060-X 11055432
81. Brunet LJ Gold GH Ngai J General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel Neuron 1996, 17(4):681-693. 10.1016/S0896-6273(00)80200-7 8893025
82. Barry PH The relative contributions of cAMP and InSP3 pathways to olfactory responses in vertebrate olfactory receptor neurons and the specificity of odorants for both pathways Journal of General Physiology 2003, 122(3):247-250. 10.1085/jgp.200308910 12939389
83. Takeuchi H Imanaka Y Hirono J Kurahashi T Cross-adaptation between olfactory responses induced by two subgroups of odorant molecules Journal of General Physiology 2003, 122(3):255-264. 10.1085/ jgp.200308867 12939391
84. Chen S Lane AP Bock R Leinders-Zufall T Zufall F Blocking adenylyl cyclase inhibits olfactory generator currents induced by "IP(3)-odors" J Neurophysiol 2000, 84(1):575-580. 10899229
85. Eisthen HL Phylogeny of the Vomeronasal System and of Receptor Cell-Types in the Olfactory and Vomeronasal Epithelia of Vertebrates Microsc Rese Tech 1992, 23(1):1-21. 10.1002/jemt.1070230102
86. Carter-Dawson LD LaVail MM Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy J Comp Neurol 1979, 188(2):245-262. 10.1002/cne.901880204 500858
87. Lee RD Thomas CF Marietta RG Stark WS Vitamin A, visual pigments, and visual receptors in Drosophila Microsc Res Tech 1996, 35(6):418-430. 10.1002/(SICI)1097-0029(19961215)35:6<418::AID-JEMT2>3.0.CO;2-E 9016446
88. Menini A Picco C Firestein S Quantal-Like Current Fluctuations Induced by Odorants in Olfactory Receptor-Cells Nature 1995, 373(6513):435-437. 10.1038/373435a0 7830795
89. Gold GH Lowe G Single Odorant Molecules Nature 1995, 376(6535):27-27. 10.1038/376027a0 7646719
90. Lowe G Gold GH Olfactory Transduction Is Intrinsically Noisy Proceedings of the National Academy of Sciences of the United States of America 1995, 92(17):7864-7868. 41246 7544007 10.1073/pnas.92.17.7864
91. Angioy AM Desogus A Barbarossa IT Anderson P Hansson BS Extreme sensitivity in an olfactory system Chemical Senses 2003, 28(4):279-284. 10.1093/chemse/28.4.279 12771014
92. Henderson SR Reuss H Hardie RC Single photon responses in Drosophila photoreceptors and their regulation by Ca2+ J Physiol 2000, 524(1):179-194. 10.1111/j.1469-7793.2000.00179.x 10747191
93. Scott K Zuker CS Assembly of the Drosophila phototransduction cascade into a signalling complex shapes elementary responses Nature 1998, 395(6704):805-808. 10.1038/27448 9796815
94. Firestein S A code in the nose Sci STKE 2004, 2004(227):pE15. 10.1126/ stke.2272004pe15 15069207
95. Spehr M Leinders-Zufall T One neuron - multiple receptors: Increased complexity in olfactory coding? Sci STKE 2005, 2005(285):pE25. 10.1126/ stke.2852005pe25 15914726
96. Porter J Anand T Johnson B Khan RM Sobel N Brain mechanisms for extracting spatial information from smell Neuron 2005, 47(4):581-592. 10.1016/j.neuron.2005.06.028 16102540
97. Gottfried JA A truffle in the mouth is worth two in the bush: Odor localization in the human brain Neuron 2005, 47(4):473-476. 10.1016/ j.neuron.2005.08.002 16102528
98. Small DM Gerber JC Mak YE Hummel T Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans Neuron 2005, 47(4):593-605. 10.1016/j.neuron.2005.07.022 16102541
99. Hepper PG Wells DL How many footsteps do dogs need to determine the direction of an odour trail? Chem Senses 2005, 30(4):291-298. 10.1093/ chemse/bji023 15741595
100. Rajan R Clement JP Bhalla US Rats smell in stereo Science 2006, 311(5761):666-670. 10.1126/science.1122096 16456082
101. Prettyjohns KN Imaging Arrays, Solid State Encyclopedia of physical science and technology 1992, 7:797-810.
102. Kleene SJ High-gain, low-noise amplification in olfactory transduction Biophysical Journal 1997, 73(2):1110-1117. 1181007 9251827
103. Lowe G Gold GH Nonlinear Amplification by Calcium-Dependent Chloride Channels in Olfactory Receptor-Cells Nature 1993, 366(6452):283-286. 10.1038/366283a0 8232590
104. Lowe G Gold GH Nonlinear Amplification by Calcium-Dependent Chloride Channels in Olfactory Receptor-Cells Biophysical Journal 1994, 66(2):A100-a100.
105. Franks KM Isaacson JS Strong single-fiber sensory inputs to olfactory cortex: Fmplications: for olfactory coding Neuron 2006, 49(3):357-363. 10.1016/j.neuron.2005.12.026 16446140
106. Mori K Nagao H Yoshihara Y The olfactory bulb: Coding and processing of odor molecule information Science 1999, 286(5440):711-715. 10.1126/ science.286.5440.711 10531048
107. Mombaerts P Wang F Dulac C Chao SK Nemes A Mendelsohn M Edmondson J Axel R Visualizing an olfactory sensory map Cell 1996, 87(4):675-686. 10.1016/ S0092-8674(00)81387-2 8929536
108. Lowe G Gold GH Olfactory transduction is intrinsically noisy Chemical Senses 1995, 20(6):174-174.
109. Ahn SM Freeman WJ Neural Dynamics under Noise in Olfactory System Biological Cybernetics 1975, 17(3):165-168. 10.1007/BF00364165 1125343
110. Cain WS Noise at Nose - Limitations on Olfactory Discrimination Bulletin of the Psychonomic Society 1976, 8(4):249-249.
111. Kleene SJ Larsson HP Lecar H Noise analysis of cAMP- and Ca2+-gated channels in isolated olfactory cilia Chemical Senses 1995, 20(6):143-143.
112. Arendt D Evolution of eyes and photoreceptor cell types International Journal of Developmental Biology 2003, 47(7-8):563-571. 14756332
113. Arendt D Tessmar-Raible K Snyman H Dorresteijn AW Wittbrodt J Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain Science 2004, 306(5697):869-871. 10.1126/science.1099955 15514158
114. Hattar S Liao HW Takao M Berson DM Yau KW Melanopsin-containing retinal. ganglion cells: Architecture, projections, and intrinsic photosensitivity Science 2002, 295(5557):1065-1070. 10.1126/ science.1069609 11834834
115. Pak WL Grossfie J White NV Nonphototactic Mutants in a Study of Vision of Drosophila Nature 1969, 222(5191):351. 10.1038/222351a0 5782110
116. Bloomquist BT Shortridge RD Schneuwly S Perdew M Montell C Steller H Rubin G Pak WL Isolation of a Putative Phospholipase-C Gene of Drosophila, Norpa, and Its Role in Phototransduction Cell 1988, 54(5):723-733. 10.1016/S0092-8674(88)80017-5 2457447
117. Montell C Visual transduction in Drosophila Annu Rev Cell Dev Biol 1999, 15:231-268. 10.1146/annurev.cellbio.15.1.231 10611962
118. Montell C TRP channels in Drosophila photoreceptor cells J Physiol 2005, 567(Pt 1):45-51. 1474165 15961416 10.1113/jphysiol.2005.092551
119. Montell C Rubin GM Molecular Characterization of the Drosophila Trp Locus - a Putative Integral Membrane-Protein Required for Phototransduction Neuron 1989, 2(4):1313-1323. 10.1016/ 0896-6273(89)90069-X 2516726
120. Jiang HP Lyubarsky A Dodd R Vardi N Pugh E Baylor D Simon MI Wu DQ Phospholipase C beta 4 is involved in modulating the visual response in mice Proceedings of the National Academy of Sciences of the United States of America 1996, 93(25):14598-14601. 26179 8962098 10.1073/ pnas.93.25.14598
121. Isoldi MC Rollag M Castrucci AM Provencio I Melanopsin signals through a phosphoinositide pathway Investigative Ophthalmology & Visual Science 2005:46.
122. Isoldi MC Rollag MD Castrucci AMD Provencio I Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin Proc Natl Acad Sci U S A 2005, 102(4):1217-1221. 545850 15653769 10.1073/ pnas.0409252102
123. Panda S Nayak SK Campo B Walker JR Hogenesch JB Jegla T Illumination of the melanopsin signaling pathway Science 2005, 307(5709):600-604. 10.1126/science.1105121 15681390
124. Qiu XD Kumbalasiri T Carlson SM Wong KY Krishna V Provencio I Berson DM Induction of photosensitivity by heterologous expression of melanopsin Nature 2005, 433(7027):745-749. 10.1038/nature03345 15674243
125. Hattar S Kumar M Park A Tong P Tung J Yau KW Berson DM Central projections of melanopsin-expressing retinal ganglion cells in the mouse J Comp Neurol 2006, 497(3):326-349. 10.1002/cne.20970 16736474
126. Hattar S Liao HW Takao M Berson DM Yau KW Melanopsin-containing retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity Science 2002, 295(5557):1065-1070. 10.1126/ science.1069609 11834834
127. Lange K Microvillar Ca++ signaling: A new view of an old problem Journal of Cellular Physiology 1999, 180(1):19-34. 10.1002/ (SICI)1097-4652(199907)180:1<19::AID-JCP3>3.0.CO;2-K 10362014
128. Martin TFJ PI(4,5)P-2 regulation of surface membrane traffic Current Opinion in Cell Biology 2001, 13(4):493-499. 10.1016/ S0955-0674(00)00241-6 11454457
129. Hansen GH Immerdal L Thorsen E Niels-Christiansen LL Nystrom BT Demant EJ Danielsen EM Lipid rafts exist as stable cholesterol-independent microdomains in the brush border membrane of enterocytes J Biol Chem 2001, 276(34):32338-32344. 10.1074/jbc.M102667200 11389144
130. Jourdan F Ultrastructural Study of Olfactory Epithelium of Rat - Occurrence of Several Morphological Types of Receptor Cells Comptes Rendus Hebdomadaires Des Seances De L Academie Des Sciences Serie D 1975, 280(4):443.
131. Moran DT Rowley JC Jafek BW Electron-Microscopy of Human Olfactory Epithelium Reveals a New Cell Type - the Microvillar Cell Brain Research 1982, 253(1-2):39-46. 10.1016/0006-8993(82)90671-0 7150975
132. Menco BPM Morrison EE Morphology of the mammalian olfactory epithelium: form, fine structure, function, and pathology Handbook of olfaction and gustation New York: Marcel Dekker Doty RL 2 2003:17-49.
133. Calof AL Mumm JS Rim PC Shou JY The neuronal stem cell of the olfactory epithelium Journal of Neurobiology 1998, 36(2):190-205. 10.1002/ (SICI)1097-4695(199808)36:2<190::AID-NEU7>3.0.CO;2-X 9712304
134. Murrell W Feron F Wetzig A Cameron N Splatt K Bellette B Bianco J Perry C Lee G Mackay-Sim A Multipotent stem cells from adult olfactory mucosa Developmental Dynamics 2005, 233(2):496-515. 10.1002/dvdy.20360 15782416
135. Caggiano M Kauer JS Hunter DD Globose Basal Cells Are Neuronal Progenitors in the Olfactory Epithelium - a Lineage Analysis Using a Replication-Incompetent Retrovirus Neuron 1994, 13(2):339-352. 10.1016/ 0896-6273(94)90351-4 8060615
136. Chen XY Fang HS Schwob JE Multipotency of purified, transplanted globose basal cells in olfactory epithelium Journal of Comparative Neurology 2004, 469(4):457-474. 10.1002/cne.11031 14755529
137. Farbman AI Buchholz JA Suzuki Y Coines A Speert D A molecular basis of cell death in olfactory epithelium J Comp Neurol 1999, 414(3):306-314. 10.1002/(SICI)1096-9861(19991122)414:3<306::AID-CNE2>3.0.CO;2-# 10516598
138. Suzuki Y Fine structural aspects of apoptosis in the olfactory epithelium J Neurocytol 2004, 33(6):693-702. 10.1007/s11068-005-3337-8 16217624
139. Suzuki Y Takeda M Obara N Suzuki N Takeichi N Olfactory epithelium consisting of supporting cells and horizontal basal cells in the posterior nasal cavity of mice Cell Tissue Res 2000, 299(3):313-325. 10.1007/s004410050030 10772246
140. Moulton DG Dynamics of cell populations in the olfactory epithelium Ann N Y Acad Sci 1974, 237(0):52-61. 10.1111/j.1749-6632.1974.tb49843.x 4214101
141. Mackay-Sim A Kittel PW On the Life Span of Olfactory Receptor Neurons Eur J Neurosci 1991, 3(3):209-215. 10.1111/j.1460-9568.1991.tb00081.x 12106197
142. Rowley JC Moran DT Jafek BW Tracer Studies of Microvillar Cells Suggest a 2Nd Morphologically Distinct Class of Sensory Neuron Exists in Mammalian Olfactory Epithelia Chemical Senses 1987, 12(4):692-692.
143. Rowley JC 3rd Moran DT Jafek BW Peroxidase backfills suggest the mammalian olfactory epithelium contains a second morphologically distinct class of bipolar sensory neuron: The microvillar cell Brain Res 1989, 502(2):387-400. 10.1016/0006-8993(89)90635-5 2819473
144. Eisthen HL Evolution of vertebrate olfactory systems Brain Behav Evol 1997, 50(4):222-233. 9310197
145. Carr VM Farbman AI Colletti LM Morgan JI Identification of a New Nonneuronal Cell Type in Rat Olfactory Epithelium Neuroscience 1991, 45(2):433-449. 10.1016/0306-4522(91)90239-K 1762687
146. Johnson EW Eller PM Jafek BW An Immunoelectron Microscopic Comparison of Olfactory Marker Protein Localization in the Supranuclear Regions of the Rat Olfactory Epithelium and Vomeronasal Organ Neuroepithelium Acta Oto-Laryngologica 1993, 113(6):766-771. 8291436
147. Iwanaga T Takahashiiwanaga H Fujita T Yamakuni T Takahashi Y Immunohistochemical Demonstration of a Cerebellar Protein (Spot-35 Protein) in Some Sensory Cells of Guinea-Pigs Biomedical Research-Tokyo 1985, 6(5):329-334.
148. Elsaesser R Montani G Tirindelli R Paysan J Phosphatidyl-inositide signalling proteins in a novel class of sensory cells in the mammalian olfactory epithelium Eur J Neurosci 2005, 21(10):2692-2700. 10.1111/ j.1460-9568.2005.04108.x 15926917
149. Costanzo RM Graziadei PPC A Quantitative-Analysis of Changes in the Olfactory Epithelium Following Bulbectomy in Hamster Journal of Comparative Neurology 1983, 215(4):370-381. 10.1002/cne.902150403 6863590
150. Graziadei GAM Experimental Studies on the Olfactory Marker Protein. 3. The Olfactory Marker Protein in the Olfactory Neuroepithelium Lacking Connections with the Forebrain Brain Research 1983, 262(2):303-308. 10.1016/0006-8993(83)91023-5 6839159
151. Michel D Moyse E Brun G Jourdan F Induction of Apoptosis in Rat Olfactory Neuroepithelium by Synaptic Target Ablation Neuroreport 1994, 5(11):1329-1332. 7919191
152. Asan E Drenckhahn D Immunocytochemical characterization of two types of microvillar cells in rodent olfactory epithelium Histochem Cell Biol 2005, 123(2):157-168. 10.1007/s00418-005-0759-4 15856279
153. Yamagishi M Ishizuka Y Fujiwara M Nakamura H Igarashi S Nakano Y Kuwano R Distribution of Calcium-Binding Proteins in Sensory Organs of the Ear, Nose and Throat Acta Otolaryngol Suppl 1993, 506:85-89. 8256606
154. Hansel DE Eipper BA Ronnett GV Regulation of olfactory neurogenesis by amidated neuropeptides Journal of Neuroscience Research 2001, 66(1):1-7. 10.1002/jnr.1191 11598996
155. Hansel DE Eipper BA Ronnett GV Neuropeptide Y functions as a neuroproliferative factor Nature 2001, 410(6831):940-944. 10.1038/ 35073601 11309620
156. Montani G Tonelli S Elsaesser R Paysan J Tirindelli R Neuropeptide Y in the olfactory microvillar cells Eur J Neurosci 2006. 16800866
157. Paysan J Bolz J Mohler H Fritschy JM Gaba(a) Receptor Alpha-1 Subunit, an Early Marker for Area Specification in Developing Rat Cerebral-Cortex Journal of Comparative Neurology 1994, 350(1):133-149. 10.1002/ cne.903500110 7860797